A spatially explicit model of sex ratio evolution in response to sex-biased dispersal

Sex-biased dispersal occurs in all seed plants and many animal species. Theoretical models have shown that sex-biased dispersal can lead to evolutionarily stable biased sex ratios. Here, we use a spatially explicit chessboard model to simulate the evolution of sex ratio in response to sex-biased dispersal range and sex-biased dispersal rate. Two life cycles are represented in the model: one in which both sexes disperse before mating (DDM), the other in which males disperse before mating and mated females or zygotes disperse after mating (DMD). Model parameters include factors like dispersal rate, dispersal range, number of individuals per patch, and habitat heterogeneity.When dispersal range is sex biased, we find that, in a homogeneous environment, the sex ratio is generally biased towards the sex that disperses more widely (sex ratio range: 0.47–0.52). In a heterogeneous environment, the sex ratio is generally biased towards the more dispersive sex in good habitats, and towards the less dispersive sex in poor habitats (sex ratio range: 0–1). This is opposite to the effect of sex-biased dispersal rate, which favours the production of the more dispersive sex in poor habitats and the less dispersive sex in good habitats (sex ratio range: 0–1). To allow for a comparison with theoretical predictions, data concerning sex-biased dispersal and habitat-dependent sex ratios should thus incorporate information about the spatial scale of both dispersal and environmental heterogeneity.     

Fluctuating sex ratios,but no sex-biased dispersal,in a promiscuous fish

Dispersal in birds and mammals tends to be female-biased in monogamous species and male-biased in polygamous species. However results for other taxa, most notably fish, are equivocal. We employed molecular markers and physical tags to test the hypothesis that Atlantic salmon, a promiscuous species with intense male-male competition for access to females, displays male-biased dispersal. We found significant variation in sex ratios and in asymmetric gene flow between neighbouring salmon populations, but little or no evidence for sex-biased dispersal. We show that conditions favouring male dispersal will often be offset by those favouring female dispersal, and that spatial and temporal variation in sex ratios within a metapopulation may favour the dispersal of different sexes in source and sink habitats. Thus, our results reconcile previous discrepancies on salmonid dispersal and highlight the need to consider metapopulation dynamics and sex ratios in the study of natal dispersal of highly fecund species.     

The ability of individuals to assess population density influences the evolution of emigration propensity and dispersal distance

We analyze the simultaneous evolution of emigration and settlement decisions for actively dispersing species differing in their ability to assess population density. Using an individual-based model we simulate dispersal as a multi-step (patch to patch) movement in a world consisting of habitat patches surrounded by a hostile matrix. Each such step is associated with the same mortality risk. Our simulations show that individuals following an informed strategy, where emigration (and settlement) probability depends on local population density, evolve a lower (natal) emigration propensity but disperse over significantly larger distances - i.e. postpone settlement longer - than individuals performing density-independent emigration. This holds especially when variation in environmental conditions is spatially correlated. Both effects can be traced to the informed individuals' ability to better exploit existing heterogeneity in reproductive chances. Yet, already moderate distance-dependent dispersal costs prevent the evolution of multi-step (long-distance) dispersal, irrespective of the dispersal strategy.     

Intersexual competition as an explanation for sex-ratio and dispersal biases in polygynous species

In polygynous mammals, it is commonly observed that both sex ratios at birth and dispersal are male biased. This has been interpreted as resulting from low female dispersal causing high female local resource competition, which would select for male-biased sex ratios. However, a female-biased sex ratio can be selected despite lower female than male-biased dispersal. This will occur if the low female dispersal is close to the optimal dispersal rate, while the male dispersal is not close to the optimal dispersal rate. The actual outcome depends on the joint evolution of sex-biased dispersal and sex ratio. Earlier analyses of joint evolution imply that there will be no sex-ratio nor dispersal biases at the joint evolutionarily stable strategy, thus they do not explain the data. However, these earlier analyses assume no intersexual competition for resources. Here, we show that when males and females compete with each other for access to resources, male-biased dispersal will be associated with male-biased birth sex ratio, as is commonly observed. A trend toward male-biased birth sex ratios is also expected if there is intersexual local resource competition and if birth sex ratio is constrained so that it cannot depart from balanced sex ratio.     

Advances in our understanding of mammalian sex-biased dispersal

Sex-biased dispersal is an almost ubiquitous feature of mammalian life history, but the evolutionary causes behind these patterns still require much clarification. A quarter of a century since the publication of seminal papers describing general patterns of sex-biased dispersal in both mammals and birds, we review the advances in our theoretical understanding of the evolutionary causes of sex-biased dispersal, and those in statistical genetics that enable us to test hypotheses and measure dispersal in natural populations. We use mammalian examples to illustrate patterns and proximate causes of sex-biased dispersal, because by far the most data are available and because they exhibit an enormous diversity in terms of dispersal strategy, mating and social systems. Recent studies using molecular markers have helped to confirm that sex-biased dispersal is widespread among mammals and varies widely in direction and intensity, but there is a great need to bridge the gap between genetic information, observational data and theory. A review of mammalian data indicates that the relationship between direction of sex-bias and mating system is not a simple one. The role of social systems emerges as a key factor in determining intensity and direction of dispersal bias, but there is still need for a theoretical framework that can account for the complex interactions between inbreeding avoidance, kin competition and cooperation to explain the impressive diversity of patterns.     

Evolution of body condition‐dependent dispersal in metapopulations

Body condition‐dependent dispersal strategies are common in nature. Although it is obvious that environmental constraints may induce a positive relationship between body condition and dispersal, it is not clear whether positive body conditional dispersal strategies may evolve as a strategy in metapopulations. We have developed an individual‐based simulation model to investigate how body condition–dispersal reaction norms evolve in metapopulations that are characterized by different levels of environmental stochasticity and dispersal mortality. In the model, body condition is related to fecundity and determined either by environmental conditions during juvenile development (adult dispersal) or by those experienced by the mother (natal dispersal). Evolutionarily stable reaction norms strongly depend on metapopulation conditions: positive body condition dependency of dispersal evolved in metapopulation conditions with low levels of dispersal mortality and high levels of environmental stochasticity. Negative body condition‐dependent dispersal evolved in metapopulations with high dispersal mortality and low environmental stochasticity. The latter strategy is responsible for higher dispersal rates under kin competition when dispersal decisions are based on body condition reached at the adult life stage. The evolution of both positive and negative body condition‐dependent dispersal strategies is consequently likely in metapopulations and depends on the prevalent environmental conditions.     

Microsatellite marker data suggest sex-biased dispersal in the common frog Rana temporaria

Despite being important models in ecological, evolutionary and conservation biology research, very little is known about the dispersal in anuran amphibians, and juvenile dispersal in particular. Using microsatellite data, we assessed signatures of sex-biased migration in the common frog (Rana temporaria) in Scandinavia. Significant heterozygosity deficiency (FIS) and lower assignment value (mAIc) among females suggest that dispersal in R. temporaria is female biased. Also variance of assignment (vAIc), estimated separately for the two sexes, was consistent with this inference, although the difference was not statistically significant. Possible proximate and ultimate explanations for female-biased dispersal in amphibians are discussed.     

Joint evolution of dispersal and connectivity

Functional connectivity, the realized flow of individuals between the suitable sites of a heterogeneous landscape, is a prime determinant of the maintenance and evolution of populations in fragmented habitats. While a large body of literature examines the evolution of dispersal propensity, it is less known how evolution shapes functional connectivity via traits that influence the distribution of the dispersers. Here, we use a simple model to demonstrate that, in a heterogeneous environment with clustered and solitary sites (i.e., with variable structural connectivity), the evolutionarily stable population contains strains that are strongly differentiated in their pattern of connectivity (local vs. global dispersal), but not necessarily in the fraction of dispersed individuals. Also during evolutionary branching, selection is disruptive predominantly on the pattern of connectivity rather than on dispersal propensity itself. Our model predicts diversification along a hitherto neglected axis of dispersal strategies and highlights the role of the solitary sites—the more isolated and therefore seemingly less important patches of habitat—in maintaining global dispersal that keeps all sites connected.     

Floral evolution and male reproductive success: Optimal dispensing schedules for pollen dispersal by animal-pollinated plants

Summary Selection favouring an outcrossing plant's ability to sire seeds generally promotes floral characters that increase (1) the frequency of pollinator visits, (2) the number of pollen grains dispersed to other plants by each pollinator and (3) the probability of a pollen grain successfully fertilizing an ovule after reaching a stigma. Flowers influence pollen dispersal and fertilization probabilities by determining the pattern of pollen removal during a series of visits (dispensing schedule). We model male reproductive success to identify optimal dispensing schedules, which characteristically involve monotonic increases in the proportion of remaining pollen removed during successive visits. These schedules balance the benefits of restricted removal, which counteracts the diminishing returns associated with animal pollination (e.g. pollinator grooming, local mate competition), with the advantages of increased removal to avoid time-dependent losses in fertilization ability (e.g. pollen precedence, declining viability). Because pollinator availability mediates this balance, the most effective dispensing schedule allows dynamic adjustment of removal to the prevailing frequency of visits experienced by individual plants. As an example of such dynamic removal we demonstrate that the dispensing mechanism ofLupinus sericeus flowers allows facultative adjustment of removal to the interval between visits. Because optimal control of pollen removal can increase a plant's mating opportunities by an order of magnitude, dispensing mechanisms should be a common component of floral design.     

Dispersal evolution diminishes the negative density dependence in dispersal

In many organisms, dispersal varies with the local population density. Such patterns of density-dependent dispersal (DDD) are expected to shape the dynamics, spatial spread, and invasiveness of populations. Despite their ecological importance, empirical evidence for the evolution of DDD patterns remains extremely scarce. This is especially relevant because rapid evolution of dispersal traits has now been empirically confirmed in several taxa. Changes in DDD of dispersing populations could help clarify not only the role of DDD in dispersal evolution, but also the possible pattern of subsequent range expansion. Here, we investigate the relationship between dispersal evolution and DDD using a long-term experimental evolution study on Drosophila melanogaster. We compared the DDD patterns of four dispersal-selected populations and their non-selected controls. The control populations showed negative DDD, which was stronger in females than in males. In contrast, the dispersal-selected populations showed DDD, where neither males nor females exhibited DDD. We compare our results with previous evolutionary predictions that focused largely on positive DDD, and highlight how the direction of evolutionary change depends on the initial DDD pattern of a population. Finally, we discuss the implications of DDD evolution for spatial ecology and evolution.     

Evolution of dispersal in metapopulations with local density dependence and demographic stochasticity

In this paper, we predict the outcome of dispersal evolution in metapopulations based on the following assumptions: (i) population dynamics within patches are density-regulated by realistic growth functions; (ii) demographic stochasticity resulting from finite population sizes within patches is accounted for; and (iii) the transition of individuals between patches is explicitly modelled by a disperser pool. We show, first, that evolutionarily stable dispersal rates do not necessarily increase with rates for the local extinction of populations due to external disturbances in habitable patches. Second, we describe how demographic stochasticity affects the evolution of dispersal rates: evolutionarily stable dispersal rates remain high even when disturbance-related rates of local extinction are low, and a variety of qualitatively different responses of adapted dispersal rates to varied levels of disturbance become possible. This paper shows, for the first time, that evolution of dispersal rates may give rise to monotonically increasing or decreasing responses, as well as to intermediate maxima or minima.     

Joint evolution of specialization and dispersal in structured metapopulations

We study the joint evolution of dispersal and specialization concerning resource usage in a mechanistically underpinned structured discrete-time metapopulation model. We show that dispersal significantly affects the evolution of specialization and that specialization is a key factor that determines the possibility of evolutionary branching in dispersal propensity. Allowing both dispersal propensity and specialization to evolve as a consequence of natural selection is necessary in order to understand the evolutionary dynamics. The joint evolution of dispersal and specialization forms a natural evolutionary path leading to the coexistence of generalists and specialists. We show that in this process, the number of different patch types and the resource distribution are essential.     

Competition between relatives and the evolution of dispersal in a parasitoid wasp

Evolutionary theory predicts that levels of dispersal vary in response to the extent of local competition for resources and the relatedness between potential competitors. Here, we test these predictions by making use of a female dispersal dimorphism in the parasitoid wasp Melittobia australica. We show that there are two distinct female morphs, which differ in morphology, pattern of egg production, and dispersal behaviour. As predicted by theory, we found that greater competition for resources resulted in increased production of dispersing females. In contrast, we did not find support for the prediction that high relatedness between competitors increases the production of dispersing females in Melittobia. Finally, we exploit the close links between the evolutionary processes leading to selection for dispersal and for biased sex ratios to examine whether the pattern of dispersal can help distinguish between competing hypotheses for the lack of sex ratio adjustment in Melittobia.     

Sex-specific fitness correlates of dispersal in a house sparrow metapopulation

1.  Dispersal affects many important ecological and evolutionary processes. Still, little is known about the fitness of dispersing individuals.
2.  Here, we use data from a long-term study of a house sparrow Passer domesticus metapopulation to compare lifetime reproductive success (LRS) of resident and immigrant individuals, all with known origin.
3.  Lifetime production of recruits by immigrant males was much lower than for resident males, because of shorter life span and lower annual mating success. In contrast, lifetime production of recruits did not differ significantly between immigrant and resident females.
4.  Over their lifetime, dispersers contributed fewer recruits to the local population than residents. This shows that immigrant house sparrows have different, sex specific, demographic effects on the population dynamics than residents.     

Negative density-dependent dispersal emerges from the joint evolution of density- and body condition-dependent dispersal strategies

Empirical studies have documented both positive and negative density-dependent dispersal, yet most theoretical models predict positive density dependence as a mechanism to avoid competition. Several hypotheses have been proposed to explain the occurrence of negative density-dependent dispersal, but few of these have been formally modeled. Here, we developed an individual-based model of the evolution of density-dependent dispersal. This model is novel in that it considers the effects of density on dispersal directly, and indirectly through effects on individual condition. Body condition is determined mechanistically, by having juveniles compete for resources in their natal patch. We found that the evolved dispersal strategy was a steep, increasing function of both density and condition. Interestingly, although populations evolved a positive density-dependent dispersal strategy, the simulated metapopulations exhibited negative density-dependent dispersal. This occurred because of the negative relationship between density and body condition: high density sites produced low-condition individuals that lacked the resources required for dispersal. Our model, therefore, generates the novel hypothesis that observed negative density-dependent dispersal can occur when high density limits the ability of organisms to disperse. We suggest that future studies consider how phenotype is linked to the environment when investigating the evolution of dispersal.     

Seasonal variation of reproductive success under female philopatry and male-biased dispersal in a common vole population

Variation of reproductive success, an important determinant of the opportunity for sexual selection, is an outcome of competition within one sex for mating with members of the other sex. In promiscuous species, males typically compete for access to females, and their reproductive strategies are strongly related to the spatial distribution of females. I used 10 microsatellite loci and the mtDNA control region to determine seasonal differences in the reproductive success of males and females of the common vole (Microtus arvalis), one of the most numerous mammals in Europe. The sex-related spatial structure and bias in dispersal between genders were also assessed. Standardized variance of the reproductive success of females did not vary seasonally due to the continuity of female philopatry throughout the breeding season and to the constancy of the number of females reproducing successfully in each season. The males are the dispersing sex, undergoing both natal and breeding dispersal. Their standardized variance of reproductive success was significantly higher than that for females in July, when only two males monopolized 80% of the females in the population and when variance of male reproductive success was highest (I_m = 7.70). The seasonally varying and high standardized variance of male reproductive success may be explained by male-male competition for matings, coupled with seasonal changes in the age structure of the population.     

Recruitment trade-offs and the evolution of dispersal mechanisms in plants

In this study we place seed size vs. seed number trade-offs in the context of plant dispersal ability. The objective was to suggest explanations for the evolution of different seed dispersal mechanisms, in particular fleshy fruits, wind dispersal and the maintenance of unassisted dispersal. We suggest that selection for improved dispersal may act either by increasing the intercept of a dispersal curve (log seed number vs. distance) or by flattening the slope of the curve. 'Improved dispersal' is defined as a marginal increase in the number of recruits sited at some (arbitrary) distance away from the parent plant. Increasing the intercept of the dispersal curve, i.e. producing more seeds, is associated with a reduction in seed size, which in turn affects the recruitment ability, provided that this ability is related to seed size. If recruitment is related to seed size there will be a recruitment cost of evolving increased seed production. On the other hand, a flattening of the slope by evolving dispersal attributes is likely to be associated with a fecundity cost. An exception is wind dispersal where smaller (and hence more numerous) seeds may lead to more efficient dispersal. We derive two main predictions: If recruitment is strongly related to seed size, selection for improved dispersal acts on the slope of the dispersal curve, i.e. by favouring evolution of dispersal attributes on seeds or fruits. If, on the other hand, recruitment is only weakly related to seed size (or not related, or negatively related), selection for improved dispersal favours increased seed production. Despite its simplicity, the model suggests explanations for (i) why so many plant species lack special seed dispersal attributes, (ii) differences in dispersal spectra among plant communities, and (iii) adaptive radiation in seed size and dispersal attributes during angiosperm evolution. This revised version was published online in July 2006 with corrections to the Cover Date.     

Unexpected collective larval dispersal but little support for sweepstakes reproductive success in the highly dispersive brooding mollusc Crepidula fornicata

In many marine invertebrates, long‐distance dispersal is achieved during an extended pelagic larval phase. Although such dispersal should result in high gene flow over broad spatial scales, fine‐scale genetic structure has often been reported, a pattern attributed to interfamilial variance in reproductive success and limited homogenization during dispersal. To examine this hypothesis, the genetic diversity of dispersing larvae must be compared with the postdispersal stages, that is benthic recruits and adults. Such data remain, however, scarce due to the difficulty to sample and analyse larvae of minute size. Here, we carried out such an investigation using the marine gastropod Crepidula fornicata. Field sampling of three to four larval pools was conducted over the reproductive season and repeated over 3 years. The genetic composition of larval pools, obtained with 16 microsatellite loci, was compared with that of recruits and adults sampled from the same site and years. In contrast to samples of juveniles and adults, large genetic temporal variations between larval pools produced at different times of the same reproductive season were observed. In addition, full‐ and half‐sibs were detected in early larvae and postdispersal juveniles, pointing to correlated dispersal paths between several pairs of individuals. Inbred larvae were also identified. Such collective larval dispersal was unexpected given the long larval duration of the study species. Our results suggest that each larval pool is produced by a small effective number of reproducers but that, over a reproductive season, the whole larval pool is produced by large numbers of reproducers across space and time.